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      Integrating Brain and Biomechanical Models—A New Paradigm for Understanding Neuro-muscular Control

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          Abstract

          To date, realistic models of how the central nervous system governs behavior have been restricted in scope to the brain, brainstem or spinal column, as if these existed as disembodied organs. Further, the model is often exercised in relation to an in vivo physiological experiment with input comprising an impulse, a periodic signal or constant activation, and output as a pattern of neural activity in one or more neural populations. Any link to behavior is inferred only indirectly via these activity patterns. We argue that to discover the principles of operation of neural systems, it is necessary to express their behavior in terms of physical movements of a realistic motor system, and to supply inputs that mimic sensory experience. To do this with confidence, we must connect our brain models to neuro-muscular models and provide relevant visual and proprioceptive feedback signals, thereby closing the loop of the simulation. This paper describes an effort to develop just such an integrated brain and biomechanical system using a number of pre-existing models. It describes a model of the saccadic oculomotor system incorporating a neuromuscular model of the eye and its six extraocular muscles. The position of the eye determines how illumination of a retinotopic input population projects information about the location of a saccade target into the system. A pre-existing saccadic burst generator model was incorporated into the system, which generated motoneuron activity patterns suitable for driving the biomechanical eye. The model was demonstrated to make accurate saccades to a target luminance under a set of environmental constraints. Challenges encountered in the development of this model showed the importance of this integrated modeling approach. Thus, we exposed shortcomings in individual model components which were only apparent when these were supplied with the more plausible inputs available in a closed loop design. Consequently we were able to suggest missing functionality which the system would require to reproduce more realistic behavior. The construction of such closed-loop animal models constitutes a new paradigm of computational neurobehavior and promises a more thoroughgoing approach to our understanding of the brain's function as a controller for movement and behavior.

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          Most cited references171

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          Neuronal circuits of the neocortex.

          We explore the extent to which neocortical circuits generalize, i.e., to what extent can neocortical neurons and the circuits they form be considered as canonical? We find that, as has long been suspected by cortical neuroanatomists, the same basic laminar and tangential organization of the excitatory neurons of the neocortex is evident wherever it has been sought. Similarly, the inhibitory neurons show characteristic morphology and patterns of connections throughout the neocortex. We offer a simple model of cortical processing that is consistent with the major features of cortical circuits: The superficial layer neurons within local patches of cortex, and within areas, cooperate to explore all possible interpretations of different cortical input and cooperatively select an interpretation consistent with their various cortical and subcortical inputs.
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            Saccade target selection and object recognition: evidence for a common attentional mechanism.

            The spatial interaction of visual attention and saccadic eye movements was investigated in a dual-task paradigm that required a target-directed saccade in combination with a letter discrimination task. Subjects had to saccade to locations within horizontal letter strings left and right of a central fixation cross. The performance in discriminating between the symbols "E" and "E", presented tachistoscopically before the saccade within the surrounding distractors was taken as a measure of visual attention. The data show that visual discrimination is best when discrimination stimulus and saccade target refer to the same object; discrimination at neighboring items is close to chance level. Also, it is not possible, in spite of prior knowledge of discrimination target position, to direct attention to the discrimination target while saccading to a spatially close saccade target. The data strongly argue for an obligatory and selective coupling of saccade programming and visual attention to one common target object. The results favor a model in which a single attentional mechanism selects objects for perceptual processing and recognition, and also provides the information necessary for motor action.
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              Synaptic organisation of the basal ganglia.

              The basal ganglia are a group of subcortical nuclei involved in a variety of processes including motor, cognitive and mnemonic functions. One of their major roles is to integrate sensorimotor, associative and limbic information in the production of context-dependent behaviours. These roles are exemplified by the clinical manifestations of neurological disorders of the basal ganglia. Recent advances in many fields, including pharmacology, anatomy, physiology and pathophysiology have provided converging data that have led to unifying hypotheses concerning the functional organisation of the basal ganglia in health and disease. The major input to the basal ganglia is derived from the cerebral cortex. Virtually the whole of the cortical mantle projects in a topographic manner onto the striatum, this cortical information is 'processed' within the striatum and passed via the so-called direct and indirect pathways to the output nuclei of the basal ganglia, the internal segment of the globus pallidus and the substantia nigra pars reticulata. The basal ganglia influence behaviour by the projections of these output nuclei to the thalamus and thence back to the cortex, or to subcortical 'premotor' regions. Recent studies have demonstrated that the organisation of these pathways is more complex than previously suggested. Thus the cortical input to the basal ganglia, in addition to innervating the spiny projection neurons, also innervates GABA interneurons, which in turn provide a feed-forward inhibition of the spiny output neurons. Individual neurons of the globus pallidus innervate basal ganglia output nuclei as well as the subthalamic nucleus and substantia nigra pars compacta. About one quarter of them also innervate the striatum and are in a position to control the output of the striatum powerfully as they preferentially contact GABA interneurons. Neurons of the pallidal complex also provide an anatomical substrate, within the basal ganglia, for the synaptic integration of functionally diverse information derived from the cortex. It is concluded that the essential concept of the direct and indirect pathways of information flow through the basal ganglia remains intact but that the role of the indirect pathway is more complex than previously suggested and that neurons of the globus pallidus are in a position to control the activity of virtually the whole of the basal ganglia.
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                Author and article information

                Contributors
                Journal
                Front Neurosci
                Front Neurosci
                Front. Neurosci.
                Frontiers in Neuroscience
                Frontiers Media S.A.
                1662-4548
                1662-453X
                06 February 2018
                2018
                : 12
                : 39
                Affiliations
                [1] 1Adaptive Behaviour Research Group, Department of Psychology, The University of Sheffield , Sheffield, United Kingdom
                [2] 2Insigneo Institute for In-Silico Medicine, The University of Sheffield , Sheffield, United Kingdom
                [3] 3Department of Electrical and Computer Engineering, The University of Patras , Patras, Greece
                [4] 4Department of Computer Science, The University of Sheffield , Sheffield, United Kingdom
                [5] 5Department of Automatic Control Systems Engineering, The University of Sheffield , Sheffield, United Kingdom
                Author notes

                Edited by: Chrystalina A. Antoniades, University of Oxford, United Kingdom

                Reviewed by: Wolfgang Stein, Illinois State University, United States; Srinivasa Chakravarthy, Indian Institute of Technology Madras, India

                *Correspondence: Kevin N. Gurney k.gurney@ 123456sheffield.ac.uk

                This article was submitted to Neuroprosthetics, a section of the journal Frontiers in Neuroscience

                Article
                10.3389/fnins.2018.00039
                5808253
                29467606
                59a8d394-b53a-43ce-847d-ef76596653bf
                Copyright © 2018 James, Papapavlou, Blenkinsop, Cope, Anderson, Moustakas and Gurney.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 01 September 2017
                : 16 January 2018
                Page count
                Figures: 15, Tables: 0, Equations: 29, References: 193, Pages: 33, Words: 26071
                Funding
                Funded by: Seventh Framework Programme 10.13039/100011102
                Award ID: 610391
                Categories
                Neuroscience
                Original Research

                Neurosciences
                integrated brain biomechanics,neuromuscular,neuromechanics,oculomotor,saccade,basal-ganglia

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